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Metagenomic Analysis of Bacterial and Fungal Communities Inhabiting Shiro Dominant Soils of Two Production Regions of Tricholoma Matsutake S

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Metagenomic Analysis of Bacterial and Fungal Communities Inhabiting Shiro Dominant Soils of Two Production Regions of Tricholoma Matsutake S Article Metagenomic Analysis of Bacterial and Fungal Communities Inhabiting Shiro Dominant Soils of Two Production Regions of Tricholoma Matsutake S. Ito & S. Imai in Korea Gi-Hong An , Jae-Han Cho, Ok-Tae Kim and Jae-Gu Han * Mushroom Research Division, National Institute of Horticultural and Herbal Science, RDA, Eumseong, Chungbuk 27709, Korea; [email protected] (G.-H.A.); [email protected] (J.-H.C.); [email protected] (O.-T.K.) * Correspondence: [email protected]; Tel.: +82-43-872-5732 Abstract: Tricholoma matsutake is an ectomycorrhizal fungus that has obligate symbiotic relationships with Pinus densiflora. Its fruiting body has a distinctive flavor and is traded at a high price. Thus, it has been a significant source of income for rural communities in Korea. We hypothesized that biotic factors considerably influence the formation of the T. matsutake mushroom, and the soils producing T. matsutake share similar microbial characteristics. Therefore, the present study aimed to detect the specific fungal and bacterial groups in T. matsutake production soils (shiro+) and nonproduction soils (shiro−) of the Bonghwa and Yanyang regions via next-generation sequencing. In a total of 15 phyla, 36 classes, 234 genera of bacteria, six phyla, 29 classes, and 164 genera of fungi were detected from four samples at both sites. The species diversity of shiro+ soils was lower than the shiro− samples in both the fungal and bacterial groups. In addition, we did not find high similarities in the microbial communities between the shiro+ soils of the two regions. However, in the resulting differences Citation: An, G.-H.; Cho, J.-H.; Kim, between the fungal communities categorized by their trophic assembly, we found a distinguishable O.-T.; Han, J.-G. Metagenomic compositional pattern in the fungal communities from the shiro+ soils and the shiro− soils of the Analysis of Bacterial and Fungal Communities Inhabiting Shiro two sites. Thus, the similarity among the microbial communities in the forest soils may be due to Dominant Soils of Two Production the fact that the microbial communities in the T. matsutake dominant soils are closely associated with Regions of Tricholoma Matsutake S. Ito biotic factors and abiotic factors such as soil properties. & S. Imai in Korea. Forests 2021, 12, 758. https://doi.org/10.3390/ Keywords: ectomycorrhizae; bacterial communities; fungal communities; metagenomics; miseq; f12060758 shiro dominant soil; Tricholoma matsutake Academic Editor: Carol A. Loopstra Received: 26 April 2021 1. Introduction Accepted: 4 June 2021 Tricholoma matsutake (S. Ito & S. Imai) that forms a symbiotic association with the Published: 9 June 2021 root tips of Pinus densiflora (Siebold & Zucc.) provides attractive commercial benefits to rural communities in Korea [1,2]. The annual yields of this mushroom are highly Publisher’s Note: MDPI stays neutral limited and unpredictable. Since it has not yet been successfully artificially cultivated, the with regard to jurisdictional claims in entire production of T. matsutake still depends upon natural harvesting from forests. In published maps and institutional affil- recent decades, many researchers have strived to succeed in the artificial production of iations. T. matsutake [2–6]. However, the artificial cultivation of this fungus has not been established. As an obligated symbiont, the biology of this mycorrhizal fungus must be considered from the perspective of the ecological interaction with the surrounding biotic factors, especially microbial groups. Copyright: © 2021 by the authors. Soil ecosystems have a wide variety of microbial communities. Microorganisms in Licensee MDPI, Basel, Switzerland. the soil can have positive or negative effects on the growth of ectomycorrhizal fungus [7]. This article is an open access article Many studies have been conducted on the microbial communities in the soils adjacent distributed under the terms and to T. matsutake [6,8–11]. The influence of the diverse microbial communities in soil on conditions of the Creative Commons the life cycle of T. matsutake, such as the development of mycelia and the formation of Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ fruiting bodies in various ways, has been investigated [4,12,13]. In particular, some soil 4.0/). bacteria, which are called mycorrhizal helper bacteria (MHB), have beneficial effects on the Forests 2021, 12, 758. https://doi.org/10.3390/f12060758 https://www.mdpi.com/journal/forests Forests 2021, 12, 758 2 of 16 mycorrhizal symbiosis by mobilizing nutrients in nutrient-deficient soils [14]. In addition, some fungi that have frequently been detected from the fruiting body and fairy ring of T. matsutake co-exist in the hyphal dominant environment as a potential mycorrhizal helper fungus [11]. Therefore, the various microbial communities associated with T. matsutake could potentially contribute to the growth of hyphae and the formation of the fruiting body of T. matsutake [7,15–17]. Recent advances in metagenomics contribute to unveiling the microbial commu- nities in various environmental samples [11,13,18]. Next-generation sequencing (NGS) based on metagenomics is a culture-independent method that enables the identification of uncultured microbes. The recent application of NGS sequencing methods, such as pyrosequencing 454 and Illumina, may provide a more direct way to detect microbial taxa, especially those with a low level of species changes [19,20]. In addition, Illumina sequencing is cost-effective and could obtain tenfold or more sequences per sample than pyrosequencing 454, thereby allowing the analysis of a high number of detailed taxonomic profiles from samples [21]. According to the report by Korean Statistical Information Service (KOSIS), the annual yields of T. matsutake in Korea dramatically decreased from 480 tons in 2007 to 140 tons in 2017. Previously, Gyeongsangbuk-do and Gangwon-do provinces were well-known as the representative T. matsutake producing regions that occupied the largest (61.3%) and second (18.0%) largest total yields of T. matsutake in Korea. However, the yields of T. matsutake in Gyeongsangbuk-do province have been gradually decreasing, and it was reported by KOSIS to be 340 tons in 2007, further decreasing to 75 tons in 2017. Thus, we speculated that the reduction in the yields of T. matsutake is due to various environmental factors, and we focused on the changes in microbial communities in the production of soils for T. matsutake. We hypothesized that the microbial communities in the production of soils for T. matsutake would be quite similar to one another, regardless of geographical characteristics, if there are microorganisms that have beneficial effects on the growth of mycelium and the formation of the fruit body of T. matsutake. Therefore, in this study, to determine the differences between the microbial communities in soils where T. matsutake occurs in Gyeongsangbuk- do and Gangwon-do provinces, we conducted sampling of the T. matsutake production soil (shiro+ soil) and nonproduction soil (shiro− soil) in two main T. matsutake production regions (Bonghwa and Yangyang) in Korea and investigated the soil bacterial and fungal communities from each sample using the Illumina Miseq sequencing platform 2. Materials and Methods 2.1. Sampling Sites Two sampling sites were mountains located near Seo-myeon, Yangyang-gun, Gangwon- do (110 m ELV, 38◦03023.8” N, 128◦38038.7” E), and Beopjeon-myeon, Bonghwa-gun, Gyeongsangbuk-do (360 m ELV, 36◦55014.2” N, 128◦56047.2” E) in south-eastern parts of the Korean peninsula. The climate and major vegetation at these sites are summarized in Table1. At the Yangyang site, in 2019, the annual mean temperature was 13.9 ◦C, and annual precipitation was 1517.3 mm. The major canopy vegetation was P. densiflora at more than 80%, and understory vegetation comprised Rhododendron schlippen (Maxim.), R. mu- cronulatum (Turcz.), Smilax nipponica (Miq.), and Carex fernaldiana (H.Lév & Vaniot). The site belongs to the public research forest under the management of the Yangyang-gun Agricul- tural Technology Center. At the Bonghwa site, in 2019, the annual mean temperature was 11.5 ◦C, and annual precipitation was 970.5 mm. The major canopy vegetation was P. densi- flora at more than 80%, and understory vegetation comprised R. schlippen, R. mucronulatum, Melampyrum roseum (Maxim.), Pteridium aquilinum (Underw. ex A. Heller), S. nipponica, and C. fernaldiana. The site in Bonghwa is privately owned. The sampling sites are geographi- cally remote, located approximately 120 km from each other (Figure1). In September 2019, soil sampling was conducted immediately after T. matsutake fruiting bodies were harvested. By using a soil sampler, soils containing shiro (shiro+) were collected at 10 cm depth from the soil surface at the three spots of the zone beneath the T. matsutake, and soils without Forests 2021, 12, x FOR PEER REVIEW 3 of 17 September 2019, soil sampling was conducted immediately after T. matsutake fruiting bod- ies were harvested. By using a soil sampler, soils containing shiro (shiro+) were collected Forests 2021, 12,at 758 10 cm depth from the soil surface at the three spots of the zone beneath the T. matsutake, 3 of 16 and soils without shiro (shiro−) were collected at approximately 3–4 m intervals from the spots with the shiro+ soils. Each soil sample was placed into a polyvinyl bag and mixed well. Shiro can beshiro distinguished (shiro−) wereby its collectedfeatures of at whitish-gray-colored approximately 3–4 m soil, intervals in which from fun- the spots with the gal hyphae are aggregatedshiro+ soils. [11]. Each Soil soil samples sample taken was placedfrom each into sampling a polyvinyl site bag were and trans- mixed well. Shiro can ported on ice andbe stored distinguished at −4 °C before by its DNA features extraction. of whitish-gray-colored soil, in which fungal hyphae are aggregated [11]. Soil samples taken from each sampling site were transported on ice and Table 1. Climates andstored vegetation at −4 ◦ofC the before experime DNAntal extraction. sites (http://www.nongsaro.go.kr/).
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